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      Gene content evolution in the arthropods

      research-article
      1 , 2 , 3 , 4 , 5 , 6 , 5 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 5 , 14 , 15 , 5 , 16 , 8 , 5 , 5 , 17 , 5 , 18 , 19 , 20 , 11 , 9 , 21 , 5 , 22 , 23 , 24 , 25 , 26 , 27 , 5 , 5 , 28 , 11 , 29 , 5 , 30 , 31 , 32 , 24 , 33 , 34 , 35 , 5 , 36 , 37 , 5 , 38 , 5 , 39 , 40 , 41 , 13 , 42 , 43 , 44 , 45 , 5 , 46 , 47 , 48 , 49 , 5 , 50 , 31 , 51 , 52 , 34 , 53 , 11 , 54 , 55 , 26 , 30 , 56 , 57 , 5 , 5 , 58 , 59 , 2 , 3 , 60 , 1 , 5 , 61 ,
      Genome Biology
      BioMed Central
      Arthropods, Genome assembly, Genomics, Protein domains, Gene content, Evolution, DNA methylation

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          Abstract

          Background

          Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods.

          Results

          Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception.

          Conclusions

          These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.

          Electronic supplementary material

          The online version of this article (10.1186/s13059-019-1925-7) contains supplementary material, which is available to authorized users.

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          Most cited references40

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          Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3.

          Current sequencing methods produce large amounts of data, but genome assemblies constructed from these data are often fragmented and incomplete. Incomplete and error-filled assemblies result in many annotation errors, especially in the number of genes present in a genome. This means that methods attempting to estimate rates of gene duplication and loss often will be misled by such errors and that rates of gene family evolution will be consistently overestimated. Here, we present a method that takes these errors into account, allowing one to accurately infer rates of gene gain and loss among genomes even with low assembly and annotation quality. The method is implemented in the newest version of the software package CAFE, along with several other novel features. We demonstrate the accuracy of the method with extensive simulations and reanalyze several previously published data sets. Our results show that errors in genome annotation do lead to higher inferred rates of gene gain and loss but that CAFE 3 sufficiently accounts for these errors to provide accurate estimates of important evolutionary parameters.
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            Is Open Access

            Redundans: an assembly pipeline for highly heterozygous genomes

            Many genomes display high levels of heterozygosity (i.e. presence of different alleles at the same loci in homologous chromosomes), being those of hybrid organisms an extreme such case. The assembly of highly heterozygous genomes from short sequencing reads is a challenging task because it is difficult to accurately recover the different haplotypes. When confronted with highly heterozygous genomes, the standard assembly process tends to collapse homozygous regions and reports heterozygous regions in alternative contigs. The boundaries between homozygous and heterozygous regions result in multiple assembly paths that are hard to resolve, which leads to highly fragmented assemblies with a total size larger than expected. This, in turn, causes numerous problems in downstream analyses such as fragmented gene models, wrong gene copy number, or broken synteny. To circumvent these caveats we have developed a pipeline that specifically deals with the assembly of heterozygous genomes by introducing a step to recognise and selectively remove alternative heterozygous contigs. We tested our pipeline on simulated and naturally-occurring heterozygous genomes and compared its accuracy to other existing tools. Our method is freely available at https://github.com/Gabaldonlab/redundans.
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              Is Open Access

              OrthoDB v9.1: cataloging evolutionary and functional annotations for animal, fungal, plant, archaeal, bacterial and viral orthologs

              OrthoDB is a comprehensive catalog of orthologs, genes inherited by extant species from a single gene in their last common ancestor. In 2016 OrthoDB reached its 9th release, growing to over 22 million genes from over 5000 species, now adding plants, archaea and viruses. In this update we focused on usability of this fast-growing wealth of data: updating the user and programmatic interfaces to browse and query the data, and further enhancing the already extensive integration of available gene functional annotations. Collating functional annotations from over 100 resources, and enabled us to propose descriptive titles for 87% of ortholog groups. Additionally, OrthoDB continues to provide computed evolutionary annotations and to allow user queries by sequence homology. The OrthoDB resource now enables users to generate publication-quality comparative genomics charts, as well as to upload, analyze and interactively explore their own private data. OrthoDB is available from http://orthodb.org.
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                Author and article information

                Contributors
                srichards@ucdavis.edu
                Journal
                Genome Biol
                Genome Biol
                Genome Biology
                BioMed Central (London )
                1474-7596
                1474-760X
                23 January 2020
                23 January 2020
                2020
                : 21
                : 15
                Affiliations
                [1 ]ISNI 0000 0001 0790 959X, GRID grid.411377.7, Department of Biology and Department of Computer Science, , Indiana University, ; Bloomington, IN USA
                [2 ]Institute for Evolution and Biodiversity, University of Münsterss, 48149 Münster, Germany
                [3 ]ISNI 0000 0001 2287 2617, GRID grid.9026.d, Institute for Bioinformatics and Chemoinformatics, , University of Hamburg, ; Hamburg, Germany
                [4 ]Westphalian University of Applied Sciences, 45665 Recklinghausen, Germany
                [5 ]ISNI 0000 0001 2160 926X, GRID grid.39382.33, Human Genome Sequencing Center, Department of Human and Molecular Genetics, , Baylor College of Medicine, ; One Baylor Plaza, Houston, TX 77030 USA
                [6 ]ISNI 0000000419368729, GRID grid.21729.3f, Present Address: Institute for Genomic Medicine, Columbia University, ; New York, NY 10032 USA
                [7 ]ISNI 0000000122986657, GRID grid.34477.33, Present Address: Howard Hughes Medical Institute, Department of Genome Sciences, , University of Washington, ; Seattle, WA 98195 USA
                [8 ]ISNI 0000 0001 2113 2895, GRID grid.483014.a, National Agricultural Library, USDA, ; Beltsville, MD 20705 USA
                [9 ]ISNI 0000 0001 2097 4943, GRID grid.213917.f, School of Biological Sciences, , Georgia Institute of Technology, ; Atlanta, GA 30332 USA
                [10 ]ISNI 0000 0004 1936 8972, GRID grid.25879.31, Present Address: Penn Epigenetics Institute, Department of Cell and Developmental Biology, , University of Pennsylvania Perelman School of Medicine, ; Philadelphia, PA 19104 USA
                [11 ]ISNI 0000 0001 2179 088X, GRID grid.1008.9, Faculty of Veterinary and Agricultural Sciences, , The University of Melbourne, ; Parkville, VIC 3010 Australia
                [12 ]GRID grid.268042.a, Department of Biology, , Washington and Lee University, ; 204 West Washington Street, Lexington, VA 24450 USA
                [13 ]ISNI 0000 0001 2179 088X, GRID grid.1008.9, School of BioSciences Science Faculty, , The University of Melbourne, ; Melbourne, VIC 3010 Australia
                [14 ]Present Address: CooperGenomics, Houston, TX USA
                [15 ]ISNI 0000 0004 1936 9043, GRID grid.259053.8, Department of Biology, , Lewis & Clark College, ; Portland, OR 97219 USA
                [16 ]ISNI 0000 0004 1936 7689, GRID grid.59062.38, Department of Plant and Soil Sciences, , University of Vermont, ; Burlington, USA
                [17 ]ISNI 0000 0004 0404 0958, GRID grid.463419.d, Beneficial Insects Introduction Research Unit, United States Department of Agriculture, , Agricultural Research Service, ; Newark, DE USA
                [18 ]ISNI 0000 0004 0461 6769, GRID grid.242287.9, Institute for Biodiversity Science and Sustainability, California Academy of Sciences, ; 55 Music Concourse Drive, San Francisco, CA 94118 USA
                [19 ]ISNI 0000 0001 1456 7807, GRID grid.254444.7, Department of Biological Sciences, , Wayne State University, ; Detroit, MI 48202 USA
                [20 ]ISNI 0000 0000 9620 1122, GRID grid.225262.3, Department of Biological Sciences, , University of Massachusetts Lowell, ; 198 Riverside Street, Lowell, MA 01854 USA
                [21 ]ISNI 0000 0004 0404 0958, GRID grid.463419.d, USDA-ARS Invasive Insect Biocontrol and Behavior Laboratory, ; Beltsville, MD USA
                [22 ]ISNI 0000 0004 0404 0958, GRID grid.463419.d, USDA-ARS, Center for Medical, Agricultural, and Veterinary Entomology, ; 1700 S.W. 23rd Drive, Gainesville, FL 32608 USA
                [23 ]ISNI 0000 0001 0699 0373, GRID grid.410590.9, Division of Insect Sciences, , National Institute of Agrobiological Sciences, ; Owashi, Tsukuba, 305-8634 Japan
                [24 ]ISNI 0000 0001 1089 1036, GRID grid.5155.4, Department of Zoology, , Institute of Biology, University of Kassel, ; 34132 Kassel, Germany
                [25 ]ISNI 0000 0004 0404 0958, GRID grid.463419.d, USDA ARS, U. S. Horticultural Research Laboratory, ; Ft. Pierce, FL 34945 USA
                [26 ]ISNI 0000 0001 2322 4988, GRID grid.8591.5, Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, , University of Geneva, ; 1211 Geneva, Switzerland
                [27 ]ISNI 0000 0004 0635 685X, GRID grid.4834.b, Present Address: Foundation for Research and Technology Hellas, , Institute of Molecular Biology and Biotechnology, ; Vassilika Vouton, 70013 Heraklion, Greece
                [28 ]ISNI 0000 0001 2150 7757, GRID grid.7849.2, Université de Lyon, Institut de Génomique Fonctionnelle de Lyon, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, ; 46 allée d’Italie, 69364 Lyon, France
                [29 ]ISNI 0000 0001 0701 8607, GRID grid.28803.31, Department of Integrative Biology, , University of Wisconsin, ; Madison, WI 53706 USA
                [30 ]ISNI 0000 0001 2168 0066, GRID grid.131063.6, Department of Biological Sciences, , University of Notre Dame, 109B Galvin Life Sciences, ; Notre Dame, IN 46556 USA
                [31 ]ISNI 0000 0001 2222 1582, GRID grid.266097.c, Department of Entomology, , University of California Riverside, ; Riverside, CA USA
                [32 ]ISNI 0000 0001 0790 959X, GRID grid.411377.7, Present Address: Department of Biology, , Indiana University, ; Bloomington, IN USA
                [33 ]ISNI 0000 0001 0726 8331, GRID grid.7628.b, Department of Biological and Medical Sciences, , Oxford Brookes University, ; Gipsy Lane, Oxford, OX3 0BP UK
                [34 ]ISNI 0000 0000 9560 654X, GRID grid.56061.34, Department of Biological Sciences, , University of Memphis, ; 3700 Walker Ave, Memphis, TN 38152 USA
                [35 ]ISNI 0000 0001 2216 5875, GRID grid.452935.c, Center for Molecular Biodiversity Research, , Zoological Research Museum Alexander Koenig, ; Bonn, Germany
                [36 ]ISNI 0000 0001 2231 4551, GRID grid.184769.5, Environmental Genomics and Systems Biology Division, , Lawrence Berkeley National Laboratory, ; Berkeley, USA
                [37 ]ISNI 0000 0004 4665 2899, GRID grid.497331.b, Present Address: Phoenix Bioinformatics, ; 39221 Paseo Padre Parkway, Ste. J., Fremont, CA 94538 USA
                [38 ]GRID grid.5963.9, Evolutionary Biology and Ecology, , Institute of Biology I (Zoology), Albert Ludwig University of Freiburg, ; 79104 Freiburg (Brsg.), Germany
                [39 ]ISNI 0000 0004 1936 8438, GRID grid.266539.d, Department of Entomology, , University of Kentucky, ; Lexington, KY 40546 USA
                [40 ]ISNI 0000 0000 8809 1613, GRID grid.7372.1, School of Life Sciences, , University of Warwick, Gibbet Hill Campus, ; Coventry, CV4 7AL UK
                [41 ]ISNI 0000 0000 8580 3777, GRID grid.6190.e, Cologne Biocenter, Zoological Institute, Department of Developmental Biology, , University of Cologne, ; 50674 Cologne, Germany
                [42 ]ISNI 0000 0001 2216 5875, GRID grid.452935.c, Centre of Taxonomy and Evolutionary Research, Arthropoda Department, , Zoological Research Museum Alexander Koenig, ; Bonn, Germany
                [43 ]ISNI 0000 0004 0386 3207, GRID grid.266685.9, School for the Environment, , University of Massachusetts Boston, ; Boston, MA 02125 USA
                [44 ]ISNI 0000 0001 2364 4210, GRID grid.7450.6, Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Abteilung für Entwicklungsbiologie, , Georg-August-Universität Göttingen, ; Göttingen, Germany
                [45 ]ISNI 0000 0001 2364 4210, GRID grid.7450.6, Göttingen Center for Molecular Biosciences (GZMB), , Georg-August-Universität Göttingen, ; Göttingen, Germany
                [46 ]ISNI 0000 0001 2173 6074, GRID grid.40803.3f, Department of Entomology and Plant Pathology, , North Carolina State University, ; Raleigh, NC 27606 USA
                [47 ]ISNI 0000 0001 2173 6074, GRID grid.40803.3f, Department of Entomology and W.M. Keck Center for Behavioral Biology, , North Carolina State University, ; Raleigh, NC 27695 USA
                [48 ]ISNI 0000 0001 2167 3675, GRID grid.14003.36, Department of Entomology, , University of Wisconsin-Madison, ; Madison, USA
                [49 ]Stored Product Insect and Engineering Research Unit, USDA-ARS Center for Grain and Animal Health Research, Manhattan, KS 66502 USA
                [50 ]ISNI 0000 0004 1936 8083, GRID grid.47894.36, Department of Biology, , Colorado State University, ; Ft. Collins, CO USA
                [51 ]ISNI 0000 0004 1936 738X, GRID grid.213876.9, Department of Entomology, , University of Georgia, ; Athens, GA USA
                [52 ]ISNI 0000 0001 2169 5989, GRID grid.252381.f, Present Address: Arkansas Biosciences Institute, Arkansas State University, ; Jonesboro, AR USA
                [53 ]ISNI 0000 0001 2112 4115, GRID grid.425585.b, Natural History Museum Vienna, ; Burgring 7, 1010 Vienna, Austria
                [54 ]ISNI 0000 0001 2112 473X, GRID grid.412234.2, INIBIOMA, Univ. Nacional del Comahue – CONICET, ; Bariloche, Argentina
                [55 ]ISNI 0000 0001 2179 9593, GRID grid.24827.3b, Department of Biological Sciences, , University of Cincinnati, ; Cincinnati, OH 45221 USA
                [56 ]ISNI 0000 0004 0404 0958, GRID grid.463419.d, Crop Production and Protection, U.S. Department of Agriculture-Agricultural Research Service, ; Beltsville, MD 20705 USA
                [57 ]ISNI 0000 0004 1936 9174, GRID grid.16416.34, Department of Biology, , University of Rochester, ; Rochester, NY 14627 USA
                [58 ]ISNI 0000 0004 1937 0538, GRID grid.9619.7, Department of Ecology, Evolution and Behavior, , The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, ; Edmond J. Safra Campus, Givat Ram, 91904 Jerusalem, Israel
                [59 ]ISNI 0000 0001 2165 4204, GRID grid.9851.5, Department of Ecology & Evolution and Swiss Institute of Bioinformatics, , University of Lausanne, ; 1015 Lausanne, Switzerland
                [60 ]ISNI 0000 0001 1014 8330, GRID grid.419495.4, Department Protein Evolution, , Max Planck Institute for Developmental Biology, ; Tübingen, Germany
                [61 ]ISNI 0000 0004 1936 9684, GRID grid.27860.3b, Present Address: UC Davis Genome Center, , University of California, ; Davis, CA 95616 USA
                Author information
                http://orcid.org/0000-0001-8959-5466
                Article
                1925
                10.1186/s13059-019-1925-7
                6977273
                31969194
                ff8ec5f0-cb57-4d15-917d-54d9c5c6940d
                © The Author(s). 2020

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 6 November 2019
                : 26 December 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000051, National Human Genome Research Institute;
                Award ID: U54 HG003273
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: DBI-1564611
                Award ID: 1355169
                Award Recipient :
                Funded by: Deutsche Forschungsgemeinschaft
                Award ID: 281125614 / GRK2220
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001711, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung;
                Award ID: PP00P3_170664
                Award ID: 31003A_143936
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100007917, Agricultural Research Service;
                Award ID: 15-8130-0547-CA
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: NI 1387/3-1, MI 649/12-1
                Award Recipient :
                Funded by: U.S. Department of Housing and Urban Development (US)
                Award ID: NCHHU-0007-13
                Award Recipient :
                Funded by: National Science Foundation
                Award ID: 1557864
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000879, Alfred P. Sloan Foundation;
                Award ID: 2013-5-35 MBE
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                Genetics
                arthropods,genome assembly,genomics,protein domains,gene content,evolution,dna methylation
                Genetics
                arthropods, genome assembly, genomics, protein domains, gene content, evolution, dna methylation

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